Download Ecology and Evolution of the Enigmatic Eclectus Parrot

Journal of Avian Medicine and Surgery 22(2):146–150, 2008
’ 2008 by the Association of Avian Veterinarians
Special Report
Ecology and Evolution of the Enigmatic Eclectus Parrot
(Eclectus roratus)
Robert Heinsohn, PhD
Abstract: Eclectus parrots (Eclectus roratus) exhibit a form of reversed sexual dichromatism
(plumage coloration) not found in other birds. The females are a striking vermilion and blue,
whereas the males are shiny green. Here, I summarize the major findings of a 10-year research
program conducted on a wild population of eclectus parrots on Cape York Peninsula, Australia,
aimed primarily at understanding the ecologic and evolutionary forces behind their unique
coloration. Unlike most other parrots, eclectus parrots breed polyandrously (where multiple
males mate with 1 female) and polygynandrously (where both sexes have multiple sexual
partners). Their mating system appears to be driven by a shortage of nest hollows. Females with
good nest sites are rare, and this forces males to share females. The red plumage of females acts
as a signal of nest hollow ownership, whereas the green of males allows them to be camouflaged
while foraging to feed the females and chicks. Eclectus parrots can also control the sex of their
offspring, although the reasons for this are not yet clear.
Key words: dichromatism, mating system, nest hollow, plumage color, sex allocation, avian,
eclectus parrot, Eclectus roratus
P. L. S. Muller. Females were not described until
1837, and even the best naturalists of the 19th
century such as John Gould were fooled for a
long time. It was not until 1874 that cocks and
hens of this species were finally united under the
same name.2 Despite the long-standing popularity
of eclectus parrots among aviculturalists, no field
studies of this species had been done until my
research at Iron Range National Park (Cape
York Peninsula, Australia) commenced in 1997.3
This was understandable, as few birds present the
field worker with such logistical difficulties.
Eclectus parrots live in the canopy of forests in
New Guinea, west to the Moluccas, east to the
Bismarck Archipelago and Solomon Islands, and
south to the tip of Cape York Peninsula in
northern Australia. Apart from living in such
remote locations, their nest hollows can be 20–
30 m (65–100 feet) above the ground, and they
are notoriously shy birds that fly away over the
treetops when disturbed.1
The eclectus parrot study began by investigating 3 unusual but interrelated aspects of their
biology that, if understood, promised unique
insights into the evolutionary processes shaping
this species in nature. These were their reversed
Introduction
Few birds have puzzled scientists more than the
eclectus parrot (Eclectus roratus). One of the 20th
century’s great evolutionary biologists, the late
Professor Bill Hamilton of Oxford University,
used to show a slide in his lecture series of a male
and female parrot sitting side by side. The male
was a vibrant green and the female a stunning
vermilion. Whereas evolutionary theory had
plenty to say about sexual selection producing
greater size or gorgeous coloration in one sex, it
stumbled somewhat in establishing what had
happened in this species. No other bird has sexes
so ‘‘beautified,’’ but in such different ways.
Hamilton ended his talk by declaring that when
he understood why one sex is red and the other
green, he would be ‘‘ready to die.’’
Male and female eclectus parrots are so
different they were long thought to be different
species.1 Males from the Moluccan Islands of
western Indonesia were first described in 1776 by
From the Fenner School of Environment and Society,
Australian National University, Canberra, ACT 0200, Australia.
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HEINSOHN—ECOLOGY AND EVOLUTION OF THE ECLECTUS PARROT
plumage coloration (also called reversed sexual
dichromatism), a system of shared, cooperative
breeding not normally seen in parrots, and their
apparent ability to manipulate the sex of their
young. All of these traits appear to relate to the
scarcity of nest hollows in the rainforest landscape, which leads to high competition among
both sexes for both nesting sites and mates.
Reversed Sexual Dichromatism
Brilliant plumage is typical of male birds and
reflects the differential enhancement of male
sexual traits used in competition for females.3,4
Traits that help individuals of just one sex
compete for mates are favored by the process of
sexual selection and can be divided into 2 general
categories. Bulkier size or weaponry can allow
males to fight for access to females, whereas
ornaments are used to attract female attention.
Long tails and bright colors in birds normally fit
the second category. Males are usually the most
colorful sex because females are likely to be in
short supply because of the extra work and
dangers involved during chick rearing. Males thus
compete for the chance to mate with females.3 In
an interesting twist, a handful of species are
known to have reversed sex roles in which males
incubate eggs, and females defend territories and
fight among themselves for access to males.5
These species provide the exceptions that prove
the rule because they demonstrate that the
competitive sex is the one most likely to have
bright colors. Phalaropes (Phalaropus species),
sandpipers (family Scolopacidae), and buttonquail (Turnix species) are good examples of
species with more colorful females.6
Eclectus parrots break this apparent rule
because their extreme reversed coloration is not
associated with reversed sex roles but instead with
stiff competition for rare nest hollows. Behavioral
research and analysis using spectroradiometry of
plumage colors showed that the males and females
look dissimilar because they have very different
selective pressures acting on them.7 The males face
higher predation pressure because they are the
ones that travel widely to find food, whereas the
females must compete especially hard for nesting
space. Good nest hollows in large rainforest trees
are in short supply and only occur at about 1 site/
km2.8 Unlike most parrots, the females do not join
the males in foraging for themselves and their
chicks; instead, they remain at the nest hollow and
defend it for up to 11 months each year. They
literally do not leave the nest tree during this
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period and have been observed to fight to the
death in protracted battles over this scarce
resource.7,9 In contrast to most parrots, which
are monogamous, each female eclectus parrot
mates with up to 5 males and relies on them to
bring all the food required by her and her chicks.10
Females with more males feeding them generally
have higher reproductive success.
Understanding the functions of the different
colors of males and females requires an ability to
‘‘look through’’ their eyes rather than our own.
This is important because birds have a broader
range of color vision than humans and, in
particular, can see ultraviolet (UV) coloration,
which is beyond our capabilities. The colors of
eclectus parrots were measured objectively with a
spectroradiometer and then the data were processed through a computer model that captured
the color-sensing abilities of the parrots.
Hollow-owning females sit out among the leafy
branches before commencing breeding and are
viewed by competing females against a background of green leaves. This provides the highest
possible contrast to her red and blue coloration
and acts as a powerful visual signal that the hollow
in that tree is occupied.7 For a male, the green
color usually has the opposite effect, although
with an interesting twist. The green provides
important camouflage against predators such as
peregrine falcons (Falco peregrinus) and rufus
owls (Ninox rufa) when the male is out foraging
among fruiting trees. However, it also has a
second purpose by making them very conspicuous
against the wood of the tree trunks near the nest
hollows where they compete with other males for
access to the females. The males’ green is also
laced with UV coloration, which the parrots’ eyes
can detect much better than their predators such
as hawks. Thus, the males’ colors are a clever
compromise between camouflage from their enemies when they need it and showiness to their own
kind at the nest trees.7 A fundamental difference
between the plumage types of male and female
eclectus parrots is that males can ‘‘switch’’ their
signal on and off depending on the background
they choose. In contrast, females are always bright
no matter which background they are against, but
they can escape unwanted attention from predators by retreating inside their hollows, if they are
fortunate enough to own one.
Social and Mating System
The second key aspect of the study was to use
molecular techniques to unravel the unusual
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breeding biology of eclectus parrots—in particular, their polyandrous mating system. Polyandry
is the rarest of avian mating systems and occurs
when a single female pairs with 2 or more males
during a breeding season.11 Polyandry falls into 2
distinct categories, depending on whether the
females mate sequentially with single males who
then care for the clutch alone (classic polyandry12)
or with multiple males who care for the clutch
cooperatively.13 Classic polyandry entails sex role
reversal with all or most parental care given by
males and aggressive competition between females for territories and mates. Typically, as soon
as 1 clutch is laid, the male assumes incubation
duties and the female seeks to lay further clutches
with additional males.6
In contrast, cooperative polyandry occurs when
2 or more males form stable social units with
single females and share paternity in a single
brood or season. In some species it appears that
groups of males can defend territories better than
a lone male, and that the benefits from sharing
paternity can outweigh the costs.14–16 In others,
space use can differ between the sexes, with
variable mating systems arising depending on the
extent of overlap of male and female territories.17–19
In both circumstances, the mating system can
become polygynandrous if the males mate with
additional females.
The numbers of males observed feeding female
eclectus parrots was much larger (up to 7 males
per female) than any other polyandrous mating
system,9 and it has also been established that their
sex roles are not reversed, as is generally the case
for reverse dichromatic birds (see above).
Throughout the long period in which females
guard their hollows, all of their food is provided
by the males, who forage for fruit over large home
ranges of approximately 30 km2. Multiple matings have been observed in quick succession, with
little apparent aggression between rival males, but
in other cases, males fight vigorously for access to
the females.9
Molecular markers known as DNA microsatellites were used to establish the extent of kinship
between the attending males. Microsatellites map
out variable loci present in nuclear DNA from
blood samples and are especially useful for
identifying close family members, such as siblings
and parents and offspring. Importantly, the data
showed that the social groups are not composed
of family members, which rules out any possibility that the extra males are grown offspring that
have failed to disperse. Instead, it appears that all
group males are seeking direct reproduction.
Although most broods of 2 nestlings had just 1
father, further group males became fathers in
later nesting attempts, and some males only
gained paternity at irregular intervals with the
same female over multiple years. For example, 1
male sired 2 different young with the same female,
but these were 7 years apart.10
Radio-tracking from light aircraft also showed
that males had very large home ranges that
encompassed many nest trees. Known individual
males were observed to spend time with several
different females, and the molecular data indeed
confirmed that some became fathers at very
widely dispersed nest trees (the maximum distance
recorded was 7.2 km).10 The authors thus concluded that the eclectus mating system regularly
includes both polyandry (females mate with more
than 1 male) and polygynandry (males mate with
more than 1 female and females mate with more
than 1 male). Both types of mating system are
very rare among parrots, and the polygynandrous
component described for eclectus parrots is
played out over the largest distances recorded
for any bird. DNA collected from feathers left in
the nest also confirmed that females monopolize
their breeding hollows over multiple years; 2
females retained their nest hollows exclusively for
the entire 8-year study period.10
Biased Sex Allocation
The final key aspect of this study has been to
investigate the apparent ability of eclectus parrots
to manipulate the sex of their offspring. The
females typically lay 2 eggs but often only manage
to fledge 1 of their chicks. Although the overall
sex ratio of fledglings is close to 50:50, some
captive females that were brought to my attention
produced long unbroken runs of 1 sex over many
clutches before switching to producing the other
sex. The maximum from 1 female was 20 sons in a
row before she switched to producing daughters.
A statistical analysis showed that these long runs
of 1 sex of offspring were highly improbable
under the assumption that males and females are
produced in equal numbers, as happens for most
birds and mammals.20
Evolutionary theory predicts various benefits
to parents of producing 1 sex of offspring over the
other, but clear examples in birds have been rare.
The few reported instances suggest that parents
might produce 1 sex earlier in the season if it helps
that sex begin breeding earlier in its life (ie,
kestrels, Falco species),21 or they might vary the
order of the sexes within a clutch if that helps 1
HEINSOHN—ECOLOGY AND EVOLUTION OF THE ECLECTUS PARROT
sex to survive better (ie, kookaburras, Dacelo
species).22 In perhaps the most celebrated example
of the ability to bias offspring sex, Seychelles
warblers (Acrocephalus sechellensis) in small
family groups have been shown to produce the
sex (females) that stays and helps raise further
broods but to produce the dispersing sex (males)
when conditions are too crowded.23
Before analyzing the mating system, it was
believed that the social groups observed around
each nest tree comprised parents with their grown
offspring, and it was hypothesized that the
parents used their ability to manipulate the sex
of offspring to skew output toward males because
they help at the nest. However, the finding that
the additional males are all unrelated to the
breeders and likely to father chicks suggests
different reasons for biased sex allocation.10 This
component of the long-term study has not yet
been analyzed, but the current working hypothesis is that breeding females only produce male
offspring, which are larger and hence more
energetically expensive, when they have good
hollows and many mates feeding them.
Conclusion
Each of the unusual traits of the eclectus parrot
discussed here is ultimately linked to the scarcity
of their nesting hollows. Field observations have
also shown that the hollows they use vary
markedly in quality. Some are low in smaller
trees and therefore prone to ground-based predators such as monitor lizards (family Varanidae)
or scrub pythons (Morelia amethistina), and many
are also prone to flooding in heavy rain. If a
hollow floods easily, then the period when it is
useable could be very short. I have observed even
large chicks drown in the torrential downpours
that occur mid-breeding season.9 In eclectus
parrots, a rare combination of intense competition between females for breeding resources, the
separation of parental duties and therefore
selective pressures on the sexes, and the effects
of trying to hide from predators appear to have
pushed these birds away from a monogamous
mating system and the monomorphic colors
found in most parrots. Instead, they have evolved
a ‘‘free-for-all’’ polygynandrous mating system
and totally divergent plumage colors in the males
and females. Although theory successfully predicts the direction of sexually selected colors in
most species, eclectus parrots show that bright
coloration can evolve independently and simultaneously in both sexes.
149
Acknowledgments: I thank Michelle Hall, Anjeli
Nathan, David Wilson, and especially Clare Blackman
and Sarah Legge for their essential help in the field, and
Peter and Emma Huybers for their generous logistical
support over the entire period of this study. This
research was supported by grants from the Australian
Research Council, National Geographic Society, and
the Winifred Violet Scott Foundation. All research
described here was conducted under license from the
ANU Animal Ethics Committee and adhered to the
Association for the Study of Animal Behavior Guidelines for the Use of Animals in Research.
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